Sulfide Toxicity as Key Control on Anaerobic Oxidation of Methane in Eutrophic Coastal Sediments.

Coastal zones account for 75% of marine methane emissions, despite covering only 15% of the ocean surface area. In these ecosystems, the tight balance between methane production and oxidation in sediments prevents most methane from escaping into seawater. However, anthropogenic activities could disrupt this balance, leading to an increased methane escape from coastal sediments. To quantify and unravel potential mechanisms underlying this disruption, we used a suite of biogeochemical and microbiological analyses to investigate the impact of anthropogenically induced redox shifts on methane cycling in sediments from three sites with contrasting bottom water redox conditions (oxic-hypoxic-euxinic) in the eutrophic Stockholm Archipelago. Our results indicate that the methane production potential increased under hypoxia and euxinia, while anaerobic oxidation of methane was disrupted under euxinia. Experimental, genomic, and biogeochemical data suggest that the virtual disappearance of methane-oxidizing archaea at the euxinic site occurred due to sulfide toxicity. This could explain a near 7-fold increase in the extent of escape of benthic methane at the euxinic site relative to the hypoxic one. In conclusion, these insights reveal how the development of euxinia could disrupt the coastal methane biofilter, potentially leading to increased methane emissions from coastal zones.

Anthropogenic Forcing of the Baltic Sea Thallium Cycle.

Anthropogenic activities have fundamentally changed the chemistry of the Baltic Sea. According to results reported in this study, not even the thallium (Tl) isotope cycle is immune to these activities. In the anoxic and sulfidic ("euxinic") East Gotland Basin today, Tl and its two stable isotopes are cycled between waters and sediments as predicted based on studies of other redox-stratified basins (e.g., the Black Sea and Cariaco Trench). The Baltic seawater Tl isotope composition (ε205Tl) is, however, higher than predicted based on the results of conservative mixing calculations. Data from a short sediment core from East Gotland Basin demonstrates that this high seawater ε205Tl value originated sometime between about 1940 and 1947 CE, around the same time other prominent anthropogenic signatures begin to appear in the same core. This juxtaposition is unlikely to be coincidental and suggests that human activities in the surrounding area have altered the seawater Tl isotope mass-balance of the Baltic Sea.

Cable bacteria delay euxinia and modulate phosphorus release in coastal hypoxic systems.

Cable bacteria are long, filamentous bacteria with a unique metabolism involving centimetre-scale electron transport. They are widespread in the sediment of seasonally hypoxic systems and their metabolic activity stimulates the dissolution of iron sulfides (FeS), releasing large quantities of ferrous iron (Fe2+) into the pore water. Upon contact with oxygen, Fe2+ oxidation forms a layer of iron(oxyhydr)oxides (FeOx), which in its turn can oxidize free sulfide (H2S) and trap phosphorus (P) diffusing upward. The metabolism of cable bacteria could thus prevent the release of H2S from the sediment and reduce the risk of euxinia, while at the same time modulating P release over seasonal timescales. However, experimental support for this so-called 'iron firewall hypothesis' is scarce. Here, we collected natural sediment in a seasonally hypoxic basin in three different seasons. Undisturbed sediment cores were incubated under anoxic conditions and the effluxes of H2S, dissolved iron (dFe) and phosphate (PO4 3-) were monitored for up to 140 days. Cores with recent cable bacterial activity revealed a high stock of sedimentary FeOx, which delayed the efflux of H2S for up to 102 days. Our results demonstrate that the iron firewall mechanism could exert an important control on the prevalence of euxinia and regulate the P release in coastal oceans.

Lipid biomarkers recording marine microbial community structure changes through the Frasnian-Famennian mass extinction event.

Studying the response and recovery of marine microbial communities during mass extinction events provides an evolutionary window through which to understand the adaptation and resilience of the marine ecosystem in the face of significant environmental disturbances. The goal of this study is to reconstruct changes in the marine microbial community structure through the Late Devonian Frasnian-Famennian (F-F) transition. We performed a multiproxy investigation on a drill core of the Upper Devonian New Albany Shale from the Illinois Basin (western Kentucky, USA). Aryl isoprenoids show green sulfur bacteria expansion and associated photic zone euxinia (PZE) enhancement during the F-F interval. These changes can be attributed to augmented terrigenous influxes, as recorded collectively by the long-chain/short-chain normal alkane ratio, carbon preference index, C30 moretane/C30 hopane, and diahopane index. Hopane/sterane ratios reveal a more pronounced dominance of eukaryotic over prokaryotic production during the mass extinction interval. Sterane distributions indicate that the microalgal community was primarily composed of green algae clades, and their dominance became more pronounced during the F-F interval and continued to rise in the subsequent periods. The 2α-methylhopane index values do not show an evident shift during the mass extinction interval, whereas the 3ß-methylhopane index values record a greater abundance of methanotrophic bacteria during the extinction interval, suggesting enhanced methane cycling due to intensified oxygen depletion. Overall, the Illinois Basin during the F-F extinction experienced heightened algal productivity due to intensified terrigenous influxes, exhibiting similarities to contemporary coastal oceans that are currently undergoing globalized cultural eutrophication. The observed microbial community shifts associated with the F-F environmental disturbances were largely restricted to the extinction interval, which suggests a relatively stable, resilient marine microbial ecosystem during the Late Devonian.

Cable Bacteria Activity Modulates Arsenic Release From Sediments in a Seasonally Hypoxic Marine Basin.

Eutrophication and global change are increasing the occurrence of seasonal hypoxia (bottom-water oxygen concentration <63 µM) in coastal systems worldwide. In extreme cases, the bottom water can become completely anoxic, allowing sulfide to escape from the sediments and leading to the development of bottom-water euxinia. In seasonally hypoxic coastal basins, electrogenic sulfur oxidation by long, filamentous cable bacteria has been shown to stimulate the formation of an iron oxide layer near the sediment-water interface, while the bottom waters are oxygenated. Upon the development of bottom-water anoxia, this iron oxide "firewall" prevents the sedimentary release of sulfide. Iron oxides also act as an adsorption trap for elements such as arsenic. Arsenic is a toxic trace metal, and its release from sediments can have a negative impact on marine ecosystems. Yet, it is currently unknown how electrogenic sulfur oxidation impacts arsenic cycling in seasonally hypoxic basins. In this study, we presented results from a seasonal field study of an uncontaminated marine lake, complemented with a long-term sediment core incubation experiment, which reveals that cable bacteria have a strong impact on the arsenic cycle in a seasonally hypoxic system. Electrogenic sulfur oxidation significantly modulates the arsenic fluxes over a seasonal time scale by enriching arsenic in the iron oxide layer near the sediment-water interface in the oxic period and pulse-releasing arsenic during the anoxic period. Fluxes as large as 20 µmol m-2 day-1 were measured, which are comparable to As fluxes reported from highly contaminated sediments. Since cable bacteria are recognized as active components of the microbial community in seasonally hypoxic systems worldwide, this seasonal amplification of arsenic fluxes is likely a widespread phenomenon.

Chromium Cycling in Redox-Stratified Basins Challenges δ53Cr Paleoredox Proxy Applications.

Chromium stable isotope composition (δ53Cr) is a promising tracer for redox conditions throughout Earth's history; however, the geochemical controls of δ53Cr have not been assessed in modern redox-stratified basins. We present new chromium (Cr) concentration and δ53Cr data in dissolved, sinking particulate, and sediment samples from the redox-stratified Lake Cadagno (Switzerland), a modern Proterozoic ocean analog. These data demonstrate isotope fractionation during incomplete (non-quantitative) reduction and removal of Cr above the chemocline, driving isotopically light Cr accumulation in euxinic deep waters. Sediment authigenic Cr is isotopically distinct from overlying waters but comparable to average continental crust. New and published data from other redox-stratified basins show analogous patterns. This challenges assumptions from δ53Cr paleoredox applications that quantitative Cr reduction and removal limits isotope fractionation. Instead, fractionation from non-quantitative Cr removal leads to sedimentary records offset from overlying waters and not reflecting high δ53Cr from oxidative continental weathering.

Influence of aphotic haloclines and euxinia on organic biomarkers and microbial communities in a thalassohaline and alkaline volcanic crater lake.

Studies on microbial communities, and their associated organic biomarkers, that are found thriving in the aphotic euxinic waters in modern stratified ecosystems are scarce compared to those undertaken in euxinic photic zones. The Dziani Dzaha (Mayotte, Indian Ocean) is a tropical, saline, alkaline crater lake that has recently been presented as a modern analog of Proterozoic Oceans due to its thalassohaline classification (having water of marine origin) and specific biogeochemical characteristics. Continuous intense photosynthetic production and microbial mineralization keep most of the water column permanently aphotic and anoxic preventing the development of a euxinic (sulfidic and anoxic) photic zone despite a high sulfide/sulfate ratio and the presence of permanent or seasonal haloclines. In this study, the molecular composition of the organic matter in Lake Dziani Dzaha was investigated and compared to the microbial diversity evaluated through 16S rRNA gene amplicon sequencing, over two contrasting seasons (rainy vs. dry) that influence water column stratification. Depth profiles of organic biomarker concentrations (chlorophyll-a and lipid biomarkers) and bacterial and archaeal OTU abundances appeared to be strongly dependent on the presence of aphotic haloclines and euxinia. OTU abundances revealed the importance of specific haloalkaliphilic bacterial and archaeal assemblages in phytoplanktonic biomass recycling and the biogeochemical functioning of the lake, suggesting new haloalkaline non-phototrophic anaerobic microbial precursors for some of the lipid biomarkers. Uncultured Firmicutes from the family Syntrophomonadaceae (Clostridiales), and Bacteroidetes from the ML635J-40 aquatic group, emerged as abundant chemotrophic bacterial members in the anoxic or euxinic waters and were probably responsible for the production of short-chain n-alkenes, wax esters, diplopterol, and tetrahymanol. Halocline-dependent euxinia also had a strong impact on the archaeal community which was dominated by Woesearchaeota in the sulfide-free waters. In the euxinic waters, methanogenic Euryarchaeota from the Methanomicrobia, Thermoplasmata, and WSA2 classes dominated and were likely at the origin of common hydrocarbon biomarkers of methanogens (phytane, pentamethyl-eicosenes, and partially hydrogenated squalene).

Niche expansion for phototrophic sulfur bacteria at the Proterozoic-Phanerozoic transition.

Fossilized carotenoid hydrocarbons provide a window into the physiology and biochemistry of ancient microbial phototrophic communities for which only a sparse and incomplete fossil record exists. However, accurate interpretation of carotenoid-derived biomarkers requires detailed knowledge of the carotenoid inventories of contemporary phototrophs and their physiologies. Here we report two distinct patterns of fossilized C40 diaromatic carotenoids. Phanerozoic marine settings show distributions of diaromatic hydrocarbons dominated by isorenieratane, a biomarker derived from low-light-adapted phototrophic green sulfur bacteria. In contrast, isorenieratane is only a minor constituent within Neoproterozoic marine sediments and Phanerozoic lacustrine paleoenvironments, for which the major compounds detected are renierapurpurane and renieratane, together with some novel C39 and C38 carotenoid degradation products. This latter pattern can be traced to cyanobacteria as shown by analyses of cultured taxa and laboratory simulations of sedimentary diagenesis. The cyanobacterial carotenoid synechoxanthin, and its immediate biosynthetic precursors, contain thermally labile, aromatic carboxylic-acid functional groups, which upon hydrogenation and mild heating yield mixtures of products that closely resemble those found in the Proterozoic fossil record. The Neoproterozoic-Phanerozoic transition in fossil carotenoid patterns likely reflects a step change in the surface sulfur inventory that afforded opportunities for the expansion of phototropic sulfur bacteria in marine ecosystems. Furthermore, this expansion might have also coincided with a major change in physiology. One possibility is that the green sulfur bacteria developed the capacity to oxidize sulfide fully to sulfate, an innovation which would have significantly increased their capacity for photosynthetic carbon fixation.

The redox structure of Ediacaran and early Cambrian oceans and its controls.

The rapid diversification of early animals during the Ediacaran (635-541 Ma) and early Cambrian (ca. 541-509 Ma) has frequently been attributed to increasing oceanic oxygenation. However, the pattern of oceanic oxygenation and its relationship to early animal evolution remain in debate. In this review, we examine the redox structure of Ediacaran and early Cambrian oceans and its controls, offering new insights into contemporaneous oceanic oxygenation patterns and their role in the coevolution of environments and early animals. We review the development of marine redox models which, in combination with independent distal deep-ocean redox proxies, supports a highly redox-stratified shelf and an anoxia-dominated deep ocean during the Ediacaran and early Cambrian. Geochemical and modeling evidence indicates that the marine redox structure was likely controlled by low atmospheric O2 levels and low seawater vertical mixing rates on shelves at that time. Furthermore, theoretical analysis and increasing geochemical evidence, particularly from South China, show that limited sulfate availability was a primary control on the attenuation of mid-depth euxinia offshore, in contrast to the existing paradigm invoking decreased organic carbon fluxes distally. In light of our review, we infer that if oceanic oxygenation indeed triggered the rise of early animals, it must have done so through a shelf oxygenation which was probably driven by elevated oxidant availability. Our review calls for further studies on Ediacaran-Cambrian marine redox structure and its controls, particularly from regions outside of South China, in order to better understand the coevolutionary relationship between oceanic redox and early animals.

Microbial assemblage and palaeoenvironmental reconstruction of the 1.38 Ga Velkerri Formation, McArthur Basin, northern Australia.

The ca. 1.38 billion years (Ga) old Roper Group of the McArthur Basin, northern Australia, is one of the most extensive Proterozoic hydrocarbon-bearing units. Organic-rich black siltstones from the Velkerri Formation were deposited in a deep-water sequence and were analysed to determine their organic geochemical (biomarker) signatures, which were used to interpret the microbial diversity and palaeoenvironment of the Roper Seaway. The indigenous hydrocarbon biomarker assemblages describe a water column dominated by bacteria with large-scale heterotrophic reworking of the organic matter in the water column or bottom sediment. Possible evidence for microbial reworking includes a large unresolved complex mixture (UCM), high ratios of mid-chained and terminally branched monomethyl alkanes relative to n-alkanes-features characteristic of indigenous Proterozoic bitumen. Steranes, biomarkers for single-celled and multicellular eukaryotes, were below detection limits in all extracts analysed, despite eukaryotic microfossils having been previously identified in the Roper Group, albeit largely in organically lean shallower water facies. These data suggest that eukaryotes, while present in the Roper Seaway, were ecologically restricted and contributed little to export production. The 2,3,4- and 2,3,6-trimethyl aryl isoprenoids (TMAI) were absent or in very low concentration in the Velkerri Formation. The low abundance is primary and not caused by thermal destruction. The combination of increased dibenzothiophene in the Amungee Member of the Velkerri Formation and trace metal redox geochemistry suggests that degradation of carotenoids occurred during intermittent oxygen exposure at the sediment-water interface and/or the water column was rarely euxinic in the photic zone and likely only transiently euxinic at depth. A comparison of this work with recently published biomarker and trace elemental studies from other mid-Proterozoic basins demonstrates that microbial environments, water column geochemistry and basin redox were heterogeneous.

A stable and productive marine microbial community was sustained through the end-Devonian Hangenberg Crisis within the Cleveland Shale of the Appalachian Basin, United States.

The end-Devonian Hangenberg Crisis constituted one of the greatest ecological and environmental perturbations of the Paleozoic Era. To date, however, it has been difficult to precisely constrain the occurrence of the Hangenberg Crisis in the Appalachian Basin of the United States and thus to directly assess the effects of this crisis on marine microbial communities and paleoenvironmental conditions. Here, we integrate organic and inorganic chemostratigraphic records compiled from two discrete outcrop locations to characterize the onset and paleoenvironmental transitions associated with the Hangenberg Crisis within the Cleveland Shale member of the Ohio Shale. The upper Cleveland Shale records both positive carbon (δ13 Corg ) and nitrogen (δ15 Ntotal ) isotopic excursions, and replenished trace metal inventories with links to eustatic rise. These dual but apparently temporally offset isotope excursions may be useful for stratigraphic correlation with other productive end-Devonian epeiric marine locations. Deposition of the black shale succession occurred locally beneath a redox-stratified water column with euxinic zones, with signs of strengthening denitrification during the Hangenberg Crisis interval, but with an otherwise stable and algal-rich marine microbial community structure sustained in the surface mixed layer as ascertained by lipid biomarker assemblages. Discernible trace fossil signals in some horizons suggest, however, that bioturbation and seafloor oxygenation occurred episodically throughout this succession and highlight that geochemical proxies often fail to capture these rapid and sporadic redox fluctuations in ancient black shales. The paleoenvironmental conditions, source biota, and accumulations of black shale are consistent with expressions of the Hangenberg Crisis globally, suggesting this event is likely captured within the uppermost strata of the Cleveland Shale in North America.

Mercury isotope signatures record photic zone euxinia in the Mesoproterozoic ocean.

Photic zone euxinia (PZE) is a condition where anoxic, H2S-rich waters occur in the photic zone (PZ). PZE has been invoked as an impediment to the evolution of complex life on early Earth and as a kill mechanism for Phanerozoic mass extinctions. Here, we investigate the potential application of mercury (Hg) stable isotopes in marine sedimentary rocks as a proxy for PZE by measuring Hg isotope compositions in late Mesoproterozoic (∼1.1 Ga) shales that have independent evidence of PZE during discrete intervals. Strikingly, a significantly negative shift of Hg mass-independent isotope fractionation (MIF) was observed during euxinic intervals, suggesting changes in Hg sources or transformations in oceans coincident with the development of PZE. We propose that the negative shift of Hg MIF was most likely caused by (i) photoreduction of Hg(II) complexed by reduced sulfur ligands in a sulfide-rich PZ, and (ii) enhanced sequestration of atmospheric Hg(0) to the sediments by thiols and sulfide that were enriched in the surface ocean as a result of PZE. This study thus demonstrates that Hg isotope compositions in ancient marine sedimentary rocks can be a promising proxy for PZE and therefore may provide valuable insights into changes in ocean chemistry and its impact on the evolution of life.

Carbon and Sulfur Cycling below the Chemocline in a Meromictic Lake and the Identification of a Novel Taxonomic Lineage in the FCB Superphylum, Candidatus Aegiribacteria.

Mahoney Lake in British Columbia is an extreme meromictic system with unusually high levels of sulfate and sulfide present in the water column. As is common in strongly stratified lakes, Mahoney Lake hosts a dense, sulfide-oxidizing phototrophic microbial community where light reaches the chemocline. Below this "plate," the euxinic hypolimnion is anoxic, eutrophic, saline, and rich in sulfide, polysulfides, elemental sulfur, and other sulfur intermediates. While much is known regarding microbial communities in sunlit portions of euxinic systems, the composition and genetic potential of organisms living at aphotic depths have rarely been studied. Metagenomic sequencing of samples from the hypolimnion and the underlying sediments of Mahoney Lake indicate that multiple taxa contribute to sulfate reduction below the chemocline and that the hypolimnion and sediments each support distinct populations of sulfate reducing bacteria (SRB) that differ from the SRB populations observed in the chemocline. After assembling and binning the metagenomic datasets, we recovered near-complete genomes of dominant populations including two Deltaproteobacteria. One of the deltaproteobacterial genomes encoded a 16S rRNA sequence that was most closely related to the sulfur-disproportionating genus Dissulfuribacter and the other encoded a 16S rRNA sequence that was most closely related to the fatty acid- and aromatic acid-degrading genus Syntrophus. We also recovered two near-complete genomes of Firmicutes species. Analysis of concatenated ribosomal protein trees suggests these genomes are most closely related to extremely alkaliphilic genera Alkaliphilus and Dethiobacter. Our metagenomic data indicate that these Firmicutes contribute to carbon cycling below the chemocline. Lastly, we recovered a nearly complete genome from the sediment metagenome which represents a new genus within the FCB (Fibrobacteres, Chlorobi, Bacteroidetes) superphylum. Consistent with the geochemical data, we found little or no evidence for organisms capable of sulfide oxidation in the aphotic zone below the chemocline. Instead, comparison of functional genes below the chemocline are consistent with recovery of multiple populations capable of reducing oxidized sulfur. Our data support previous observations that at least some of the sulfide necessary to support the dense population of phototrophs in the chemocline is supplied from sulfate reduction in the hypolimnion and sediments. These studies provide key insights regarding the taxonomic and functional diversity within a euxinic environment and highlight the complexity of biogeochemical carbon and sulfur cycling necessary to maintain euxinia.

Eutrophication, microbial-sulfate reduction and mass extinctions.

In post-Cambrian time, life on Earth experienced 5 major extinction events, likely instigated by adverse environmental conditions. Biodiversity loss among marine taxa, for at least 3 of these mass extinction events (Late Devonian, end-Permian and end-Triassic), has been connected with widespread oxygen-depleted and sulfide-bearing marine water. Furthermore, geochemical and sedimentary evidence suggest that these events correlate with rather abrupt climate warming and possibly increased terrestrial weathering. This suggests that biodiversity loss may be triggered by mechanisms intrinsic to the Earth system, notably, the biogeochemical sulfur and carbon cycle. This climate warming feedback produces large-scale eutrophication on the continental shelf, which, in turn, expands oxygen minimum zones by increased respiration, which can turn to a sulfidic state by increased microbial-sulfate reduction due to increased availability of organic matter. A plankton community turnover from a high-diversity eukaryote to high-biomass bacterial dominated food web is the catalyst proposed in this anoxia-extinction scenario and stands in stark contrast to the postulated productivity collapse suggested for the end-Cretaceous mass extinction. This cascade of events is relevant for the future ocean under predicted greenhouse driven climate change. The exacerbation of anoxic "dead" zones is already progressing in modern oceanic environments, and this is likely to increase due to climate induced continental weathering and resulting eutrophication of the oceans.

Diversity of Miscellaneous Crenarchaeotic Group archaea in freshwater karstic lakes and their segregation between planktonic and sediment habitats.

The Miscellaneous Crenarchaeotic Group (MCG) is an archaeal lineage whose members are widespread and abundant in marine sediments. MCG archaea have also been consistently found in stratified euxinic lakes. In this work, we have studied archaeal communities in three karstic lakes to reveal potential habitat segregation of MCG subgroups between planktonic and sediment compartments. In the studied lakes, archaeal assemblages were strikingly similar to those of the marine subsurface with predominance of uncultured Halobacteria in the plankton and Thermoplasmata and MCG in anoxic, organic-rich sediments. Multivariate analyses identified sulphide and dissolved organic carbon as predictor variables of archaeal community composition. Quantification of MCG using a newly designed qPCR primer pair that improves coverage for MCG subgroups prevalent in the studied lakes revealed conspicuous populations in both the plankton and the sediment. Subgroups MCG-5a and -5b appear as planktonic specialists thriving in euxinic bottom waters, while subgroup MCG-6 emerges as a generalist group able to cope with varying reducing conditions. Besides, comparison of DNA- and cDNA-based pyrotag libraries revealed that rare subgroups in DNA libraries, i.e. MCG-15, were prevalent in cDNA-based datasets, suggesting that euxinic, organic-rich sediments of karstic lakes provide optimal niches for the activity of some specialized MCG subgroups.

Phototrophic sulfide oxidation: environmental insights and a method for kinetic analysis.

Previously, we presented data that indicated microbial sulfide oxidation would out-compete strictly chemical, abiotic sulfide oxidation reactions under nearly all conditions relevant to extant ecosystems (Luther et al., 2011). In particular, we showed how anaerobic microbial sulfide oxidation rates were several orders of magnitude higher than even metal catalyzed aerobic sulfide oxidation processes. The fact that biotic anaerobic sulfide oxidation is kinetically superior to abiotic reactions implies that nearly all anaerobic and sulfidic environments should host microbial populations that oxidize sulfide at appreciable rates. This was likely an important biogeochemical process during long stretches of euxinia in the oceans suggested by the geologic record. In particular, phototrophic sulfide oxidation allows the utilization of carbon dioxide as the electron acceptor suggesting that this process should be particularly widespread rather than relying on the presence of other chemical oxidants. Using the Chesapeake Bay as an example, we argue that phototrophic sulfide oxidation may be more important in many environments than is currently appreciated. Finally, we present methodological considerations to assist other groups that wish to study this process.